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Isopod Saduria Entomon

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Isopod Saduria Entomon MARINE ECOLOGY PROGRESS SERIES Vol. 103: 285-289,1994 Published January 10 Mar. Ecol. Prog. Ser. Haemolymph nitrogen compounds and ammonia efflux rates under anoxia in the brackish water isopod Saduria entomon Lars ~agerman',Anna szaniawska2 'Marine Biological Laboratory, Copenhagen University, Strandpromenaden 5. DK-3000 Helsinger, Denmark 20ceanographical Institute, Gdansk University, Al. Pilsudskiego 46, 81-378 Gdynia. Poland ABSTRACT: Production and excretion of nitrogenous end products was studied in the benthic Baltic isopod Saduria entomon (L.) under normoxic and anoxic conditions. S. entomon is ammonotelic. Normoxic haemolymph ammonia concentrations were 176 + 53 (SD) pm01 NH.,; I-' decreasing with time to 50 pm01 NH,' 1-' after 120 h anoxia. Normoxic ammonia efflux rate was 0.53 i- 0.07 (SD) pm01 NH,' g-' h-', decreasing 90% after 96 h anoxia. Normoxic haemolymph urate amounted to 135 pm01 I-', increasing after 120 h under anoxia to 741 + 79 (SD) pm01 l-' Haemolymph urate concentrations were relatively high because of the ammonia excretion and an undetectable urate excretion even under anoxia. Circulating free amino acids also increased progressively under anoxia, from the nor- moxic 28 to 165 mm01 1'' after 96 h anoxia. This increase was largely due to accumulation of alanine as a result of an anaerobic metabolism. Ammonia was calculated to be the quantitatively dominat~ng nitrogenous end product in S. entomon. An effective efflux of ammonia prevents an excessive build-up of toxic ammonia in the haemolymph. KEY WORDS: Ammonia . Amino acids . Urate . Total nitrogen . Blood . Excretion . Production INTRODUCTION sent in amounts that normally permit the species to continue an aerobic metabolism (Hagerman & Vis- The brackish water isopod Saduria entomon has mann 1993). been the subject of several ecological and physio- In ammonotelic animals, ammonia dominates amongst logical studies made in recent years (e.g. Leonardsson the nitrogenous compounds which result from protein et al. 1987, Hagerman & Szaniawska 1988, 1990, 1991, metabolism and which are excreted under normoxia. 1992, Haahtela 1990, Vismann 1991). These studies Most crustaceans are ammonotelic and also excrete have revealed S. entomon to be a most adaptable spe- lesser amounts of amino acids, urea and uric acid cies with an exceptional tolerance of anoxia and (Regnault 1987). As long as the respiratory mechan- hydrogen sulphide concentrations. The extent of its isms are maintained, the normal nitrogen metabolism tolerance to periods of anoxia or to exposure of hydro- is also maintained. It is only when the overall meta- gen sulphide whilst under anoxia is dependent on its bolic rate is impaired that nitrogen metabolism may be activity pattern which determines whether the end expected also to change and when environmental con- product of the anaerobic metabolism will be lactate or ditions worsen to severe hypoxia or anoxia, a change alanine. Lactate accumulation relates to short-term in the production and efflux of nitrogenous waste survival whilst alanine accumulation leads to long- products may occur. It has been shown that increased term survival under anoxia (Hagerman & Szaniawska production of uric acid (urate) occurs in Carcinus 1990). In the presence of hydrogen sulphide, however, rnaenas and Callinectes sapidus when exposed to S. entomon invariably switches to anaerobiosis which hypoxia (Lallier et al. 1987, DeFur et al. 1990).Further- also leads to lactate production - even if oxygen is pre- more, it has been shown that anaerobic metabolism O Inter-Research 1994 Mar. Ecol. Prog. Ser. 103: 285-289, 1994 can lead to increased haemolymph levels of amino Urate (uric acid) and urea: Haemolymph and water acids, with alanine being predominant, in Saduria urate and urea were measured using Sigma Diagnostic entornon (Hagerman & Szaniawska 1990). Kits 685 and 635 respectively. To correct for haemo- Although the respiratory responses of Saduria cyanin interference at the wavelength 520 nm a blank entomon have been studied intensively (Hagerman & absorbance measure was made on the same haemo- Szaniawska 1988, 1990, 1991, 1992),the origin and fate lymph volume as the test sample diluted in a buffer of the nitrogenous end products of this species are not identical to the one in the Sigma Kit. well known. The purpose of the present study was thus Amino acids: Amino acids in the haemolymph were to investigate ammonia efflux rates and haemolymph measured by HPLC (Jasco 880 PU) connected to a nitrogen compounds under anoxia in S. entomon. Perkin Elmer LC 1000 fluorescence detector. The ana- lytical method was pre-column (column: LiChrosorb RP18) derivatisation with orthophthalaldehyde (OPA) MATERIAL AND METHODS according to the description by Gardner & Miller (1980). Haemolymph (1 to 10 p1) was allowed to react Experimental procedure. Specimens of Saduria en- with 5 times as much OPA 2 min before injection. Indi- tomon (L.) were collected in the Gulf of Gdansk, Poland vidual amino acid calibration was made with a Sigma (S 7%) in 1991-92 and transported to the Marine Bio- amino acid calibration standard no. AA-S-18. logical Laboratory (Helsingnrr, Denmark) where they were stored at ambient temperature and salinity (T 7 "C; S 7 Yw).Specimens (except those starved for experimen- RESULTS tal purposes) were fed twice weekly with shrimp or bi- valve flesh. Anoxic conditions were maintained for up to Under normoxic conditions, the blood ammonia 120 h by bubbling the medium with N2gas. Oxygen ten- concentrations in fed Saduria entomon are very variable sion of the medium was controlled by a microprocessor- but wlth a mean of 176 F 53 (SD)pm01 NH,' 1-' (Fig. 1). controlled regulator connected to a Radiometer PHM73 The exoskeleton of S. entomon is relatively heavier than acid-base analyser supplied with a Radiometer E5046 that of many other crustaceans and we may assume that oxygen electrode. The medium was considered to be the blood volume is correspondingly a smaller propor- anoxic when oxygen tensions were < 1 Torr. The aquaria tion of the fresh body weight. If 20 % of the wet weight is were covered with small plastic spheres. This dimin- taken to be a representative value for the blood volume ished contact with atmosphere and reduced the need for (Lockwood 1968, Spaargaren 1972), then the weight- N2 bubbling considerably. Change in water pH was thus specif~c blood concentration is 0.04 to 0.05 pm01 reduced to an increase of only 0.4 pH units (from pH 8.1 NH4+ g-' wet wt. Initially there was a difference be- to 8.5). tween the blood ammonia concentrations of the fed and In experiments involving the assessment of excre- starved groups with the latter having a mean of 100 to tion, Saduria entomon were kept individually in con- 120 pm01 NH4+1-' (0.02 to 0.03 pm01 NH,' g-' wet wt). tainers with 250 m1 of the medium. These solutions These lower values in the starved specimens are pos- were kept anoxic by bubbling N2 gas through them as sibly due to a decline in protein catabolism reducing described above. Water samples were taken at timed intervals and either analysed immediately or kept frozen at -80°C untll needed for analysis. Haemolymph samples were collected by inserting a hypodermic syringe (Terumo, 100 p1) into the heart region from d dorsoposterior direction. Each individual was sampled once only. Analytical procedure. Total ammonia (NH,'): Ammonia concentrations were measured using a modi- fied flow injectiodgas diffusion technique (Clinch et al. 1988) as described by Hosie et al. (1991) and Hunter & Uglow (1993a). Water samples were injected directly into the NaOH carrier stream and blood samples (25 ,u1) 0 1 10 were diluted 1:40 before injection. The peak heights of 0 24 48 72 96 120 the chart outputs of the water and blood samples were T~mein anoxia (hours) compared with those of a series of fresh ammonium suI- Fig. 1 Saduna entomon. Haemolymph ammonia concen- phate standards in the range 5 to 25 pm01 NH,+l-l pre- trations in normoxia and as a function of t~meunder anoxia. pared daily with the medium or saline respectively. (m) pm01 l ' haemolymph; (0)pm01 g.' wet wt Hagerman & Szaniawska. Ammonia efflux by Saduna entomon under anoxia ammonia production or to starvation-induced tissue Table 1. Sadul-ia entomon. Haemolymph ammonia production shrinkage causing an increased blood volume. Blood and haemolymph ammonla replacement times ammonia levels decrease with time under anoxia and in fed isopods drop quickly over the first 24 h to values sim- Product~on Replacement time ilar to those of the starved specimens. In both fed and (pm01 g-' wet wt h-') (mln) starved groups, the mean blood ammonia values after Normoxia 0.54 120 h under anoxia had dropped to a mean of 50 pm01 24 h anoxia 0.48 NH,' 1-' (0.011 pm01 NH,+ g-' wet wt) - a >4-fold 48 h anoxia 0.37 change from normoxic values. 72 h anoxia 0.18 96 The mean normoxic weight-specific ammonia efflux h anoxia 0.1 rate was 0.53 ? 0.07 (SD) pm01 NH,' g-' h-' (Fig. 2). Efflux rates showed a wide variability and no differ- ence between the means of the starved and fed groups No urea was detected in any of the water or blood was found. The efflux rates decreased steadily after samples collected under normoxia or whilst under 24 h under anoxia and after 96 h reached 0.052 + 0.017 anoxia. Small quantities of urate were present in the (SD) pm01 ammonia g-' h-'. This represents a 90% haemolymph samples collected under normoxia and drop from original rates, corresponding to a decrease these amounted to 135 ? 21 (SD)~mol urate 1-' haemo- of 4.7 nmol h-' or 0.9 % h-' of the normoxic efflux rate. lymph (Fig. 3).The urate concentrations increased pro- The weight-specific blood ammonia concentration gressively during the anoxic period and reached 74 1 i and excretion rate can be used to derive a turnover 79 pm01 urate 1-' haemolymph (= 0.15 pm01 urate g-' ratio - the time required to effect a complete replace- wet wt) after 120 h.
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